Hidden diversity of soil giant viruses

Schulz, Frederik; Alteio, Lauren; Goudeau, Danielle; Ryan, Elizabeth M.; Yu, Feiqiao B.; Malmstrom, Rex R.; Blanchard, Jeffrey; Woyke, Tanja

doi:10.1038/s41467-018-07335-2

Title: Hidden diversity of soil giant viruses

Journal Article · 19 November 2018 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-07335-2 · OSTI ID:1510757

^[1]; Alteio, Lauren ^[2];

^[1]; Ryan, Elizabeth M. ^[1]; Yu, Feiqiao B. ^[3]; Malmstrom, Rex R. ^[1];

^[2];

^[1]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of Massachusetts, Amherst, MA (United States)
Stanford Univ., Stanford, CA (United States)

Known giant virus diversity is currently skewed towards viruses isolated from aquatic environments and cultivated in the laboratory. Here, we employ cultivation-independent metagenomics and mini-metagenomics on soils from the Harvard Forest, leading to the discovery of 16 novel giant viruses, chiefly recovered by mini-metagenomics. The candidate viruses greatly expand phylogenetic diversity of known giant viruses and either represented novel lineages or are affiliated with klosneuviruses, Cafeteria roenbergensis virus or tupanviruses. One assembled genome with a size of 2.4 Mb represents the largest currently known viral genome in the Mimiviridae, and others encode up to 80% orphan genes. In addition, we find more than 240 major capsid proteins encoded on unbinned metagenome fragments, further indicating that giant viruses are underexplored in soil ecosystems. The fact that most of these novel viruses evaded detection in bulk metagenomes suggests that mini-metagenomics could be a valuable approach to unearth viral giants.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1510757

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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High-Throughput Isolation of Giant Viruses in Liquid Medium Using Automated Flow Cytometry and Fluorescence Staining Khalil, Jacques Y. B.; Robert, Stephane; Reteno, Dorine G. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00026	journal	January 2016
Giant Viruses of Amoebas: An Update Aherfi, Sarah; Colson, Philippe; La Scola, Bernard Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00349	journal	March 2016
MG-Digger: An Automated Pipeline to Search for Giant Virus-Related Sequences in Metagenomes Verneau, Jonathan; Levasseur, Anthony; Raoult, Didier Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00428	journal	March 2016
Orpheovirus IHUMI-LCC2: A New Virus among the Giant Viruses Andreani, Julien; Khalil, Jacques Y. B.; Baptiste, Emeline Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02643	journal	January 2018
Kaumoebavirus, a New Virus That Clusters with Faustoviruses and Asfarviridae Bajrai, Leena; Benamar, Samia; Azhar, Esam Viruses, Vol. 8, Issue 11 https://doi.org/10.3390/v8110278	journal	October 2016
A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae Wilhelm, Steven; Bird, Jordan; Bonifer, Kyle Viruses, Vol. 9, Issue 3 https://doi.org/10.3390/v9030046	journal	March 2017
Ubiquitous giants: a plethora of giant viruses found in Brazil and Antarctica Andrade, Ana; Arantes, Thalita; Rodrigues, Rodrigo figshare https://doi.org/10.6084/m9.figshare.c.3986424.v1	collection	January 2018
Deciphering viral presences: two novel partial giant viruses detected in marine metagenome and in a mine drainage metagenome Andreani, Julien; Verneau, Jonathan; Raoult, Didier figshare https://doi.org/10.6084/m9.figshare.c.4065569	collection	January 2018
Microfluidic-based mini-metagenomics enables discovery of novel microbial lineages from complex environmental samples Yu, Feiqiao Brian; Blainey, Paul C.; Schulz, Frederik eLife, Vol. 6 https://doi.org/10.7554/eLife.26580	journal	July 2017
The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea Deeg, Christoph M.; Chow, Cheryl-Emiliane T.; Suttle, Curtis A. eLife, Vol. 7 https://doi.org/10.7554/eLife.33014	journal	March 2018
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015

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High-throughput isolation of giant viruses using high-content screening Francis, Rania; Ominami, Yusuke; Bou Khalil, Jacques Yaacoub Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0475-6	journal	June 2019
A single-cell genome perspective on studying intracellular associations in unicellular eukaryotes Tyml, Tomáš; Date, Shailesh V.; Woyke, Tanja Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1786 https://doi.org/10.1098/rstb.2019.0082	journal	October 2019
Advancing Genome-Resolved Metagenomics beyond the Shotgun Malmstrom, Rex R.; Eloe-Fadrosh, Emiley A. mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00118-19	journal	June 2019
Distribution of SNSs in Mimivirus Genomes and the Classification of Mimiviruses Isolated from Japan Akashi, Motohiro; Takemura, Masaharu Microbes and Environments, Vol. 34, Issue 4 https://doi.org/10.1264/jsme2.me19077	journal	January 2019
Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere Rolland, Clara; Andreani, Julien; Louazani, Amina Viruses, Vol. 11, Issue 4 https://doi.org/10.3390/v11040312	journal	March 2019
Giant Viruses—Big Surprises Brandes, Nadav; Linial, Michal Viruses, Vol. 11, Issue 5 https://doi.org/10.3390/v11050404	journal	April 2019
Virophages of Giant Viruses: An Update at Eleven Mougari, Said; Sahmi-Bounsiar, Dehia; Levasseur, Anthony Viruses, Vol. 11, Issue 8 https://doi.org/10.3390/v11080733	journal	August 2019
Additional file 1 of Unraveling the habitat preferences, ecological drivers, potential hosts, and auxiliary metabolism of soil giant viruses across China Liang, Jie-Liang; Feng, Shi-wei; Jia, Pu figshare https://doi.org/10.6084/m9.figshare.26353256	dataset	January 2024
Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world Jeudy, Sandra; Bertaux, Lionel; Alempic, Jean-Marie The ISME Journal, Vol. 14, Issue 3 https://doi.org/10.1038/s41396-019-0565-y	journal	December 2019
The DNA methylation landscape of giant viruses Jeudy, Sandra; Rigou, Sofia; Alempic, Jean-Marie Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16414-2	journal	May 2020
High-throughput isolation of giant viruses using high-content screening Francis, Rania; Ominami, Yusuke; Bou Khalil, Jacques Yaacoub Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0475-6	journal	June 2019
A new marseillevirus isolated in Southern Brazil from Limnoperna fortunei dos Santos, Raíssa Nunes; Campos, Fabrício Souza; Medeiros de Albuquerque, Nathalia Rammé Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35237	journal	October 2016
On the occurrence of cytochrome P450 in viruses Lamb, David C.; Follmer, Alec H.; Goldstone, Jared V. Proceedings of the National Academy of Sciences, Vol. 116, Issue 25 https://doi.org/10.1073/pnas.1901080116	journal	June 2019
A single-cell genome perspective on studying intracellular associations in unicellular eukaryotes Tyml, Tomáš; Date, Shailesh V.; Woyke, Tanja Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1786 https://doi.org/10.1098/rstb.2019.0082	journal	October 2019
Targeted metagenomic recovery of four divergent viruses reveals shared and distinctive characteristics of giant viruses of marine eukaryotes Needham, David M.; Poirier, Camille; Hehenberger, Elisabeth Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 374, Issue 1786 https://doi.org/10.1098/rstb.2019.0086	journal	October 2019
Untapped viral diversity in global soil metagenomes Graham, Emily B.; Paez-Espino, David; Brislawn, Colin BioRxiv https://doi.org/10.1101/583997	posted_content	January 2019
Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust Van Goethem, Marc W.; Swenson, Tami L.; Trubl, Gareth mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mbio.02287-19	journal	December 2019
Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere Rolland, Clara; Andreani, Julien; Louazani, Amina Viruses, Vol. 11, Issue 4 https://doi.org/10.3390/v11040312	journal	March 2019
Giant Viruses—Big Surprises Brandes, Nadav; Linial, Michal Viruses, Vol. 11, Issue 5 https://doi.org/10.3390/v11050404	journal	April 2019
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